Journal of Applied Phycology

, Volume 28, Issue 1, pp 149–159 | Cite as

Changes in phytochemical content and pharmacological activities of three Chlorella strains grown in different nitrogen conditions

  • Adeyemi O. Aremu
  • Nqobile A. Masondo
  • Zoltan Molnár
  • Wendy A. Stirk
  • Vince Ördög
  • Johannes Van Staden
Article

Abstract

The phytochemical content and biological activity of three Chlorella strains cultured in low (35 mg L−1) or high (700 mg L−1) nitrogen (N) and harvested on days 5 and 10 were evaluated. High N resulted in a higher biomass in Chlorella MACC 438 and MACC 452 while MACC 555 produced a higher biomass in low N. MACC 555 (low N/day 5) had the highest phenolic content, and MACC 438 in low N/day 5 and high N/day 5 accumulated the highest flavonoids and condensed tannins, respectively. Iridoids were most abundant in MACC 452 on low N/day 10. Harvest time had the greatest effect on the phytochemical content with phenolics, flavonoids, and condensed tannins decreasing over time and iridoids increasing in low N and decreasing in high N conditions. Extracts were more active in β-carotene-linoleic acid model compared to 2,2-diphenyl-1-picrylhydrazyl (DPPH) free radical scavenging assay. Most extracts had good antimicrobial activity. Extracts became less potent over time in the antioxidant, acetylcholinesterase inhibitory (AChE), and antimicrobial assays when growing in low N and more potent in the antioxidant and AChE assays when grown in high N. Thus, phytochemical content and biological activities of the three Chlorella strains were affected by N levels, harvest time, and strain.

Keywords

Acetylcholinesterase Antimicrobial Antioxidant Chlorophyta Microalgae Natural products 

References

  1. Abedin RMA, Taha HM (2008) Antibacterial and antifungal activity of cyanobacteria and green microalgae. Evaluation of medium components by Plackett-Burman design for antimicrobial activity of Spirulina platensis. Glob J Biotech Biochem 3:22–31Google Scholar
  2. Amaro HM, Guedes CA, Malcata FX (2011) Antimicrobial activites of microalgae: an invited review. In: Méndez-Vilas A (ed) Science against microbial pathogens: communicating current research and technological advances. Formatex Research Center, Badajoz, Spain, pp 1272–1280Google Scholar
  3. Aremu AO, Bairu MW, Szüčová L, Doležal K, Finnie JF, Van Staden J (2012) Assessment of the role of meta-topolins on in vitro produced phenolics and acclimatization competence of micropropagated ‘Williams’ banana. Acta Physiol Plant 34:2265–2273CrossRefGoogle Scholar
  4. Aremu AO, Masondo NA, Stirk WA, Ördög V, Van Staden J (2014) Influence of culture age on the phytochemical content and pharmacological activities of five Scenedesmus strains. J Appl Phycol 26:407–415CrossRefGoogle Scholar
  5. Aremu AO, Ndhlala AR, Fawole OA, Light ME, Finnie JF, Van Staden J (2010) In vitro pharmacological evaluation and phenolic content of ten South African medicinal plants used as anthelmintics. S Afr J Bot 76:558–566CrossRefGoogle Scholar
  6. Balasundram N, Sundram K, Samman S (2006) Phenolic compounds in plants and agri-industrial by-products: Antioxidant activity, occurrence, and potential uses. Food Chem 99:191–203CrossRefGoogle Scholar
  7. Batista AP, Gouveia L, Bandarra NM, Franco JM, Raymundo A (2013) Comparison of microalgal biomass profiles as novel functional ingredient for food products. Algal Res 2:164–173CrossRefGoogle Scholar
  8. Bhagavathy S, Sumathi P, Jancy Sherene Bell I (2011) Green algae Chlorococcum humicola-a new source of bioactive compounds with antimicrobial activity. Asian Pacific J Trop Biomed 1:S1–S7CrossRefGoogle Scholar
  9. Borowitzka MA (1995) Microalgae as sources of pharmaceuticals and other biologically active compounds. J Appl Phycol 7:3–15CrossRefGoogle Scholar
  10. Borowitzka MA (2013) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756CrossRefGoogle Scholar
  11. Brennan L, Owende P (2010) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energy Rev 14:557–577CrossRefGoogle Scholar
  12. Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306CrossRefPubMedGoogle Scholar
  13. Coesel SN, Baumgartner AC, Teles LM, Ramos AA, Henriques NM, Cancela L, Varela JCS (2008) Nutrient limitation is the main regulatory factor for carotenoid accumulation and for Psy and Pds steady state transcript levels in Dunaliella salina (Chlorophyta) exposed to high light and salt stress. Mar Biotechnol 10:602–611CrossRefPubMedGoogle Scholar
  14. Custódio L, Justo T, Silvestre L, Barradas A, Duarte CV, Pereira H, Barreira L, Rauter AP, Alberício F, Varela J (2012) Microalgae of different phyla display antioxidant, metal chelating and acetylcholinesterase inhibitory activities. Food Chem 131:134–140CrossRefGoogle Scholar
  15. Custódio L, Soares F, Pereira H, Barreira L, Vizetto-Duarte C, Rodrigues MJ, Rauter AP, Alberício F, Varela J (2014a) Fatty acid composition and biological activities of Isochrysis galbana T-ISO, Tetraselmis sp. and Scenedesmus sp.: possible application in the pharmaceutical and functional food industries. J Appl Phycol 26:151–161CrossRefGoogle Scholar
  16. Custódio L, Soares F, Pereira H, Rodrigues MJ, Barreira L, Rauter AP, Alberício F, Varela J (2014b) Botryococcus braunii and Nannochloropsis oculata extracts inhibit cholinesterases and protect human dopaminergic SH-SY5Y cells from H2O2-induced cytotoxicity. JAppl Phycol. doi:10.1007/s10811-014-0369-4 Google Scholar
  17. Duval B, Shetty K, Thomas WH (1999) Phenolic compounds and antioxidant properties in the snow alga Chlamydomonas nivalis after exposure to UV light. J Appl Phycol 11:559–566CrossRefGoogle Scholar
  18. Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95CrossRefPubMedGoogle Scholar
  19. Eloff JN (1998) A sensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria. Planta Med 64:711–713CrossRefPubMedGoogle Scholar
  20. Franco D, Sineiro J, Rubilar M, Sánchez M, Jerez M, Pinelo M, Costoya N, Núñez MJ (2008) Polyphenols from plant materials: extraction and antioxidant power. Electr J Env Agric Food Chem 7:3210–3216Google Scholar
  21. Gaffney M, O'Rourke R, Murphy R (2014) Manipulation of fatty acid and antioxidant profiles of the microalgae Schizochytrium sp. through flaxseed oil supplementation. Algal Res 6:195–200CrossRefGoogle Scholar
  22. Ghasemi Y, Moradian A, Mohagheghzadeh A, Shokravi S, Morowvat MH (2007) Antifungal and antibacterial activity of the microalgae collected from paddy fields of Iran: characterization of antimicrobial activity of Chroococcus dispersus. J Biol Sci 7:904–910CrossRefGoogle Scholar
  23. Goiris K, Muylaert K, Fraeye I, Foubert I, Brabanter J, Cooman L (2012) Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. J Appl Phycol 24:1477–1486CrossRefGoogle Scholar
  24. Goiris K, Van Colen W, Wilches I, León-Tamariz F, De Cooman L, Muylaert K (2015) Impact of nutrient stress on antioxidant production in three species of microalgae. Algal Res 7:51–57CrossRefGoogle Scholar
  25. Grierson S, Strezov V, Bengtsson J (2013) Life cycle assessment of a microalgae biomass cultivation, bio-oil extraction and pyrolysis processing regime. Algal Res 2:299–311CrossRefGoogle Scholar
  26. Griffiths MJ, Hille RP, Harrison SL (2012) Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions. J Appl Phycol 24:989–1001CrossRefGoogle Scholar
  27. Gülçin İ (2012) Antioxidant activity of food constituents: an overview. Arch Toxicol 86:345–391CrossRefPubMedGoogle Scholar
  28. Hajimahmoodi M, Faramarzi M, Mohammadi N, Soltani N, Oveisi M, Nafissi-Varcheh N (2010) Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae. J Appl Phycol 22:43–50CrossRefGoogle Scholar
  29. Hempel N, Petrick I, Behrendt F (2012) Biomass productivity and productivity of fatty acids and amino acids of microalgae strains as key characteristics of suitability for biodiesel production. J Appl Phycol 24:1407–1418CrossRefPubMedPubMedCentralGoogle Scholar
  30. Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agric Food Chem 53:1841–1856CrossRefPubMedGoogle Scholar
  31. Huang X, Huang Z, Wen W, Yan J (2013) Effects of nitrogen supplementation of the culture medium on the growth, total lipid content and fatty acid profiles of three microalgae (Tetraselmis subcordiformis, Nannochloropsis oculata and Pavlova viridis). J Appl Phycol 25:129–137CrossRefGoogle Scholar
  32. Klein B, Walter C, Lange H, Buchholz R (2012) Microalgae as natural sources for antioxidative compounds. J Appl Phycol 24:1133–1139CrossRefGoogle Scholar
  33. Kokou F, Makridis P, Kentouri M, Divanach P (2012) Antibacterial activity in microalgae cultures. Aquacult Res 43:1520–1527CrossRefGoogle Scholar
  34. Lee Y-K (2001) Microalgal mass culture systems and methods: their limitation and potential. J Appl Phycol 13:307–315CrossRefGoogle Scholar
  35. Levieille G, Wilson G (2002) In vitro propagation and iridoid analysis of the medicinal species Harpagophytum procumbens and H. zeyheri. Plant Cell Rep 21:220–225CrossRefGoogle Scholar
  36. Li H-B, Cheng K-W, Wong C-C, Fan K-W, Chen F, Jiang Y (2007) Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chem 102:771–776CrossRefGoogle Scholar
  37. Makkar HPS, Sidhuraju P, Becker K (2007) Plant secondary metabolites. Methods in molecular biology, vol 393. Humana Press Inc, New Jersey, USACrossRefGoogle Scholar
  38. Nair BB, Krishika A (2011) Antibacterial activity of freshwater microalga (Scenedesmus sp.) against three bacterial strains. J Biosci Res 2:160–165Google Scholar
  39. Ndhlala AR, Aremu AO, Moyo M, Amoo SO, Van Staden J (2012) Acetylcholineterase inhibitors from plant sources: friends or foes? In: White CJ, Tait JE (eds) Cholinesterase: production, uses and health effects. Nova, New York, pp 67–98Google Scholar
  40. Noaman NH, Fattah A, Khaleafa M, Zaky SH (2004) Factors affecting antimicrobial activity of Synechococcus leopoliensis. Microbiol Res 159:395–402CrossRefPubMedGoogle Scholar
  41. Ördög V (1982) Apparatus for laboratory algal bioassay. Int Rev Ges Hydrobiol 67:127–137Google Scholar
  42. Ördög V, Stirk W, Bálint P, Lovász C, Pulz O, Van Staden J (2013) Lipid productivity and fatty acid composition in Chlorella and Scenepdesmus strains grown in nitrogen-stressed conditions. J Appl Phycol 25:233–243CrossRefGoogle Scholar
  43. Ördög V, Stirk WA, Bálint P, Van Staden J, Lovász C (2012) Changes in lipid, protein and pigment concentrations in nitrogen-stressed Chlorella minutissima cultures. J Appl Phycol 24:907–914CrossRefGoogle Scholar
  44. Ördög V, Stirk WA, Lenobel R, Bancířová M, Strnad M, Van Staden J, Szigeti J, Németh L (2004) Screening microalgae for some potentially useful agricultural and pharmaceutical secondary metabolites. J Appl Phycol 16:309–314CrossRefGoogle Scholar
  45. Pirastru L, Darwish M, Chu F, Perreault F, Sirois L, Sleno L, Popovic R (2012) Carotenoid production and change of photosynthetic functions in Scenedesmus sp. exposed to nitrogen limitation and acetate treatment. J Appl Phycol 24:117–124CrossRefGoogle Scholar
  46. Prakash JW, Antonisamy JM, Jeeva S (2011) Antimicrobial activity of certain fresh water microalgae from Thamirabarani River, Tamil Nadu, South India. Asian Pacific J Trop Biomed 1:S170–S173CrossRefGoogle Scholar
  47. Prior RL, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53:4290–4302CrossRefPubMedGoogle Scholar
  48. Robles Centeno PO, Ballantine DL (1999) Effects of culture conditions on production of antibiotically active metabolites by the marine alga Spyridia filamentosa (Ceramiaceae, Rhodophyta). I. Light. J Appl Phycol 11:217–224CrossRefGoogle Scholar
  49. Shanab SMM, Mostafa SSM, Shalaby EA, Mahmoud GI (2012) Aqueous extracts of microalgae exhibit antioxidant and anticancer activities. Asian Pacific J Trop Biomed 2:608–615CrossRefGoogle Scholar
  50. Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96CrossRefPubMedGoogle Scholar
  51. Stirk WA, Bálint P, Tarkowská D, Novák O, Maróti G, Ljung K, Turečková V, Strnad M, Ördög V, van Staden J (2014) Effect of light on growth and endogenous hormones in Chlorella minutissima (Trebouxiophyceae). Plant Physiol Biochem 79:66–76CrossRefPubMedGoogle Scholar
  52. Varfolomeev SD, Wasserman LA (2011) Microalgae as source of biofuel, food, fodder, and medicines. Appl Biochem Microbiol 47:789–807CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Adeyemi O. Aremu
    • 1
  • Nqobile A. Masondo
    • 1
  • Zoltan Molnár
    • 2
  • Wendy A. Stirk
    • 1
  • Vince Ördög
    • 1
    • 2
  • Johannes Van Staden
    • 1
  1. 1.Research Centre for Plant Growth and Development, School of Life SciencesUniversity of KwaZulu-Natal PietermaritzburgScottsvilleSouth Africa
  2. 2.Institute of Plant Biology, Faculty of Agricultural and Food ScienceUniversity of West HungaryMosonmagyaróvárHungary

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